Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-26T13:52:43.860Z Has data issue: false hasContentIssue false
  • English
  • Français

Seasonal feeding activity of the tree-hole tick, Ixodes arboricola

Published online by Cambridge University Press:  21 March 2014

D. J. A. HEYLEN ,
A. R. VAN OOSTEN ,
N. DEVRIENDT ,
J. ELST ,
L. DE BRUYN  and
E. MATTHYSEN
D. J. A. HEYLEN*
Affiliation:
Evolutionary Ecology Group, Department of Biology, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium
A. R. VAN OOSTEN
Affiliation:
Evolutionary Ecology Group, Department of Biology, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium
N. DEVRIENDT
Affiliation:
Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
J. ELST
Affiliation:
Evolutionary Ecology Group, Department of Biology, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium
L. DE BRUYN
Affiliation:
Evolutionary Ecology Group, Department of Biology, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium Research Institute for Nature and Forest (INBO), Kliniekstraat 25, 1070 Brussels, Belgium
E. MATTHYSEN
Affiliation:
Evolutionary Ecology Group, Department of Biology, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium
*
* Corresponding author: Evolutionary Ecology Group, Department of Biology, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium. E-mail: Dieter.Heylen@uantwerpen.be
Get access Rights & Permissions [Opens in a new window]

Summary

Bird-specific ticks do not infest humans and livestock, but these ticks often share their avian hosts with generalist ticks that do. Therefore, their feeding activity may have an impact on the transmission of pathogens outside bird–tick transmission cycles. Here we examined the seasonal feeding activity of the tree-hole tick (Ixodes arboricola) in relation to the activity of its hole-breeding hosts (Parus major and Cyanistes caeruleus). We analysed data on ticks derived from birds, on the abundance of engorged ticks inside nest boxes, and on bird nests that were experimentally exposed to ticks. We observed a non-random pattern of feeding associated with the tick instar and host age. The majority of adult ticks fed on nestlings, while nymphs and larvae fed on both free-flying birds and nestlings. Due to their fast development, some ticks were able to feed twice within the same breeding season. The highest infestation rates in free-flying birds were found during the pre-breeding period and during autumn and winter when birds roost inside cavities. Except during winter, feeding of I. arboricola overlapped in time with the generalist Ixodes ricinus, implying that tick-borne microorganisms that are maintained by I. arboricola and birds could be bridged by I. ricinus to other hosts.

Keywords

Ixodes arboricolaIxodes ricinusphenologyBorreliaRickettsiaLyme borreliosis
Type
Research Article
Information
Parasitology , Volume 141 , Issue 8 , July 2014 , pp. 1044 - 1051
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arthur, D. R. (1963). British Ticks. Butterworths, London, UK.Google Scholar
Balashov, Y. S. (1972). Bloodsucking ticks (Ixodidea) – vectors of diseases of man and animals. Miscellaneous Publications of the Entomological Society of America 8, 159–376.Google Scholar
Bown, K. J., Begon, M., Bennett, M., Birtles, R. J., Burthe, S., Lambin, X., Telfer, S., Woldehiwet, Z. and Ogden, N. H. (2006). Sympatric Ixodes trianguliceps and Ixodes ricinus ticks feeding on field voles (Microtus agrestis): potential for increased risk of Anaplasma phagocytophilum in the United Kingdom? Vector-Borne and Zoonotic Diseases 6, 404–410.Google Scholar
Comstedt, P., Bergstrom, S., Olsen, B., Garpmo, U., Marjavaara, L., Mejlon, H., Barbour, A. G. and Bunikis, J. (2006). Migratory passerine birds as reservoirs of Lyme borreliosis in Europe. Emerging Infectious Diseases 12, 1087–1095.Google Scholar
Cramp, S. and Perrins, C. M. (1993). Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Paleartic, pp. 255–281. Oxford University Press, Oxford, UK.Google Scholar
Donohue, K. V., Khalil, S. M. S., Ross, E., Mitchell, R. D., Roe, R. M. and Sonenshine, D. E. (2009). Male engorgement factor: role in stimulating engorgement to repletion in the ixodid tick, Dermacentor variabilis . Journal of Insect Physiology 55, 909–918.Google Scholar
Dunn, H. E. (1975). The timing of endothermy in the development of altrical birds. The Condor 77, 288–293.Google Scholar
Gallizzi, K., Bischoff, L. L., Gern, L. and Richner, H. (2008). An experimental study on the influence of tick infestations on nestling performance in Great Tits (Parus major). The Auk 125, 915–922.Google Scholar
Gern, L. and Rais, O. (1996). Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). Journal of Medical Entomology 33, 189–192.Google Scholar
Gosler, A. (1993). The Great Tit. Hamlyn, London, UK.Google Scholar
Gray, J. S. (1991). The development and seasonal activity of the tick Ixodes ricinus: a vector of Lyme borreliosis. Review of Medical and Veterinary Entomology 79, 323–333.Google Scholar
Gray, J. S. (1998). The ecology of ticks transmitting Lyme borreliosis. Experimental and Applied Acarology 22, 249–258.Google Scholar
Heylen, D. J. A. (2011). Parasite-host interactions between ticks and hole-breeding songbirds. PhD dissertation, Antwerp.Google Scholar
Heylen, D. J. A. and Matthysen, E. (2010). Contrasting detachment strategies in two congeneric ticks (Ixodidae) parasitizing the same songbird. Parasitology 137, 661–667.Google Scholar
Heylen, D. J. A. and Matthysen, E. (2011). Differential virulence in two congeneric ticks infesting songbird nestlings. Parasitology 138, 1011–1021.Google Scholar
Heylen, D., Adriaensen, F., Dauwe, T., Eens, M. and Matthysen, E. (2009). Offspring quality and tick infestation load in brood rearing great tits Parus major . Oikos 118, 1499–1506.Google Scholar
Heylen, D. J. A., Madder, M. and Matthysen, E. (2010). Lack of resistance against the tick Ixodes ricinus in two related passerine bird species. International Journal for Parasitology 40, 183–191.Google Scholar
Heylen, D. J. A., White, J., Elst, J., Jacobs, I., van de Sande, C. and Matthysen, E. (2012). Nestling development and the timing of tick attachments. Parasitology 139, 766–773.CrossRefGoogle ScholarPubMed
Heylen, D., Adriaensen, F., Van Dongen, S., Sprong, H. and Matthysen, E. (2013 a). Ecological factors that determine Ixodes ricinus tick burdens in the great tit (Parus major), an important avian reservoir of Borrelia burgdorferi s.l. International Journal for Parasitology 43, 603–611.Google Scholar
Heylen, D., Matthysen, E., Fonville, M. and Sprong, H. (2013 b). Songbirds as general transmitters but selective amplifiers of Borrelia burgdorferi sensu lato genotypes in Ixodes rinicus ticks. Environmental Microbiology. doi:10.1111/1462–2920.12304. Google ScholarPubMed
Heylen, D., Tijsse, E., Fonville, M., Matthysen, E. and Sprong, H. (2013 c). Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community. Environmental Microbiology 15, 663–673.Google Scholar
Heylen, D., Sprong, H., van Oers, K., Fonville, M., Leirs, H. and Matthysen, E. (in press). Are terrestrial bird-specialized ticks competent vectors for Borrelia burgdorferi s.l.? Environmental Microbiology.Google Scholar
Hillyard, P. D. (1996). Ticks of North-West Europe. Backhuys Publishers, London, UK.Google Scholar
Hinde, R. A. (1952). The behaviour of the Great Tit (Parus major) and some other related species. Behaviour 2, 1–201.Google Scholar
Hudde, H. and Walter, G. (1988). Verbreitung und Wirtswahl der Vogelzecke Ixodes arboricola (Ixodoidea, Ixodidae) in der Bundesrepublik Deutschland. Vogelwarte 34, 201–207.Google Scholar
Kluijver, H. N. (1951). The population ecology of the Great Tit, Parus m. major L. Ardea 39, 1–135.Google Scholar
Liebisch, G. (1996). Biology and life cycle of Ixodes (Pholeoixodes) arboricola Schulze and Schlottke, 1929 (Ixodidae). In Acarology IX, Vol. 1 (ed. Mitchell, R., Horn, D. J., Needham, G. R. and Welbourn, W. C.), pp. 453–455. The Ohio Biological Survey, Columbus, OH, USA.Google Scholar
Literak, I., Kocianova, E., Dusbabek, F., Martinu, J., Podzemny, P. and Sychra, O. (2007). Winter infestation of wild birds by ticks and chiggers (Acari : Ixodidae, Trombiculidae) in the Czech Republic. Parasitology Research 101, 1709–1711.Google Scholar
Matthysen, E., Adriaensen, F. and Dhondt, A. A. (2001). Local recruitment of great and blue tits (Parus major, P. caeruleus) in relation to study plot size and degree of isolation. Ecography 24, 33–42.Google Scholar
Matthysen, E., Adriaensen, F. and Dhondt, A. A. (2011). Multiple responses to increasing spring temperatures in the breeding cycle of blue and great tits (Cyanistes caeruleus, Parus major). Global Change Biology 17, 1–16.Google Scholar
Mejlon, H. A. and Jaenson, T. G. T. (1997). Questing behaviour of Ixodes ricinus (Acari: Ixodidae). Experimental and Applied Acarology 21, 247–255.Google Scholar
Mertens, J. A. L. (1969). The influence of brood size on the energy metabolism and water loss of nestling great tits Parus major major . Ibis 111, 11–16.CrossRefGoogle Scholar
Molenberghs, G. and Verbeke, G. (2005). Models for Discrete Longitudinal Data. Springer-Verlag, New York, NY, USA.Google Scholar
Nilsson, S. G. (1984). The evolution of nest-site selection among hole-nesting birds: the importance of nest predation and competition. Ornis Scandinavica 15, 167–175.Google Scholar
Norte, A. C., Ramos, J. A., Gern, L., Núncio, M. S. and Lopes de Carvalho, I. (2013). Birds as reservoirs for Borrelia burgdorferi s.l. in Western Europe: circulation of B. turdi and other genospecies in bird-tick cycles in Portugal. Environmental Microbiology 15, 386–397.Google Scholar
Perrins, C. M. (1979). British Tits. Collins, London, UK.Google Scholar
Piesman, J. and Gern, L. (2004). Lyme borreliosis in Europe and North America. Parasitology 129, S191–S220.Google Scholar
Randolph, S. E. (2004). Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as a vector. Parasitology 129, 37–65.Google Scholar
Randolph, S. E., Gern, L. and Nuttall, P. A. (1996). Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitology Today 12, 472–479.Google Scholar
Randolph, S. E., Green, R. M., Hoodless, A. N. and Peacey, M. F. (2002). An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus . International Journal for Parasitology 32, 979–989.Google Scholar
Rechav, Y., Goldberg, M. and Fielden, L. J. (1997). Evidence for attachment pheromones in the Cayenne tick (Acari: Ixodidae). Journal of Medical Entomology 34, 234–237.Google Scholar
Sonenshine, D. E. (2004). Pheromones and other semiochemicals of ticks and their use in tick control. Parasitology 129, S405–S425.Google Scholar
Spitalska, E., Literak, I., Kocianova, E. and Taragel'ova, V. (2011). The importance of Ixodes arboricola in transmission of Rickettsia spp., Anaplasma phagocytophilum, and Borrelia burgdorferi sensu lato in the Czech Republic, Central Europe. Vector-Borne and Zoonotic Diseases 11, 1235–1241.Google Scholar
Thorud, C. (1999). Experimentelle Infektion der Vogelzecke Ixodes (Pholeoixodes) arboricola mit Borrelia burgdorferi sensu lato. PhD dissertation, Hannover.Google Scholar
Tyller, Z., Paclik, M. and Remes, V. (2012). Winter night inspections of nest boxes affect their occupancy and reuse for roosting by cavity nesting birds. Acta Ornithologica 47, 79–85.Google Scholar
Ulmanen, I., Saikku, P., Vikberg, P. and Sorjonen, J. (1977). Ixodes lividus (Acari) in sand martin colonies in Fennoscandia. Oikos 28, 20–26.CrossRefGoogle Scholar
Van Overveld, T., Adriaensen, F. and Matthysen, E. (2011). Postfledging family space use in great tits in relation to environmental and parental characteristics. Behavioral Ecology 22, 899–907.Google Scholar
Visser, M. E., Adriaensen, F., van Balen, J. H., Blondel, J., Dhondt, A. A., van Dongen, S., du Feu, C., Ivankina, E. V., Kerimov, A. B., de Laet, J., Matthysen, E., McCleery, R., Orell, M. and Thomson, D. L. (2003). Variable responses to large-scale climate change in European Parus populations. Proceedings of the Royal Society B – Biological Sciences 270, 367–372.Google Scholar
Walter, G., Liebisch, A. and Streichert, J. (1979). Untersuchungen zur Biologie und Verbreitung von Zecken (Ixodoidea, Ixodidae) in Norddeutschland. Angewandete Ornithologie 5, 65–73.Google Scholar
Weiss, B. L. and Kaufman, W. R. (2004). Two feeding-induced proteins from the male gonad trigger engorgement of the female tick Amblyomma hebraeum . Proceedings of the National Academy of Sciences USA 101, 5874–5879.Google Scholar
White, J., Heylen, D. J. A. and Matthysen, E. (2012). Adaptive timing of detachment in a tick parasitizing hole-nesting birds. Parasitology 139, 264–270.Google Scholar
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. and Smith, G. M. (2009). Mixed Effect Models and Extensions in Ecology with R. Springer-Verlag, New York.Google Scholar